1887

Abstract

Colorectal cancer (CRC) is one of the most common cancers worldwide. Multiple risk factors are involved in CRC development, including age, genetics, lifestyle, diet and environment. Of these, the role of the gut microbiota in cancer biology is increasingly recognized.

Micro-organisms have been widely detected in stool samples, but few mucosal samples have been detected and sequenced in depth.

Analysis of cultured mucosal bacteria from colorectal cancer and adjacent normal mucosal tissues with metagenomics sequencing.

Twenty-eight paired tumour and non-tumour tissues from 14 patients undergoing surgery for CRC were analysed. We removed the influence of eukaryotic cells via culture. The composition of mucosal microbiota in intestinal mucosa were detected and analysed with metagenomic sequencing.

Compared with non-cultured mucosal sample, 80 % bacteria species could be detected after culture. Moreover, after culture, additional 30 % bacteria could be detected, compared with non-cultured samples. Since after culture it was difficult to estimate the original abundance of microbiome, we focused on the identification of the CRC tissue-specific species. There were 298 bacterial species, which could only be cultured and detected in CRC tissues. and could be isolated from all the tumour samples of 14 CRC patients, suggesting that these species may be related to tumour occurrence and development. Further functional analysis indicated that bacteria from CRC tissues showed more active functions, including basic metabolism, signal transduction and survival activities.

We used a new method based on culture to implement information on prokaryotic taxa, and related functions, which samples were from colorectal tissues. This method is suitable for removing eukaryotic contamination and detecting micro-organisms from other tissues.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001523
2022-04-25
2022-07-06
Loading full text...

Full text loading...

References

  1. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A et al. Global patterns and trends in colorectal cancer incidence and mortality. Gut 2017; 66:683–691 [View Article] [PubMed]
    [Google Scholar]
  2. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst 2013; 105:1907–1911 [View Article] [PubMed]
    [Google Scholar]
  3. Brennan CA, Garrett WS, Microbiota G. Gut microbiota, inflammation, and colorectal cancer. Annu Rev Microbiol 2016; 70:395–411 [View Article] [PubMed]
    [Google Scholar]
  4. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 2014; 12:661–672 [View Article] [PubMed]
    [Google Scholar]
  5. Zackular JP, Baxter NT, Chen GY, Schloss PD et al. Manipulation of the gut microbiota reveals role in colon tumorigenesis. mSphere 2016; 1:e00001-15 [View Article] [PubMed]
    [Google Scholar]
  6. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012; 22:292–298 [View Article] [PubMed]
    [Google Scholar]
  7. Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science 2017; 358:1443–1448 [View Article] [PubMed]
    [Google Scholar]
  8. Dejea CM, Fathi P, Craig JM, Boleij A, Taddese R et al. Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 2018; 359:592–597 [View Article] [PubMed]
    [Google Scholar]
  9. Ardito CM, Grüner BM, Takeuchi KK, Lubeseder-Martellato C, Teichmann N et al. EGF receptor is required for KRAS-induced pancreatic tumorigenesis. Cancer Cell 2012; 22:304–317 [View Article] [PubMed]
    [Google Scholar]
  10. Feng Q, Liang S, Jia H, Stadlmayr A, Tang L et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 2015; 6:6528 [View Article] [PubMed]
    [Google Scholar]
  11. Yu J, Feng Q, Wong SH, Zhang D, Liang QY et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 2017; 66:70–78 [View Article] [PubMed]
    [Google Scholar]
  12. Flemer B, Lynch DB, Brown JMR, Jeffery IB, Ryan FJ et al. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 2017; 66:633–643 [View Article] [PubMed]
    [Google Scholar]
  13. Lazarevic V, Whiteson K, Gaïa N, Gizard Y, Hernandez D et al. Analysis of the salivary microbiome using culture-independent techniques. J Clin Bioinforma 2012; 2:4 [View Article] [PubMed]
    [Google Scholar]
  14. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011; 12:R60 [View Article] [PubMed]
    [Google Scholar]
  15. Johnson CM, Wei C, Ensor JE, Smolenski DJ, Amos CI et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control 2013; 24:1207–1222 [View Article] [PubMed]
    [Google Scholar]
  16. Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL et al. The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 2009; 125:171–180 [View Article] [PubMed]
    [Google Scholar]
  17. Song M, Garrett WS, Chan AT. Nutrients, foods, and colorectal cancer prevention. Gastroenterology 2015; 148:1244–1260 [View Article] [PubMed]
    [Google Scholar]
  18. Garrett WS. The gut microbiota and colon cancer. Science 2019; 364:1133–1135 [View Article] [PubMed]
    [Google Scholar]
  19. Zhu W, Miyata N, Winter MG, Arenales A, Hughes ER et al. Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer. J Exp Med 2019; 216:2378–2393 [View Article] [PubMed]
    [Google Scholar]
  20. Brennan CA, Garrett WS. Fusobacterium nucleatum - symbiont, opportunist and oncobacterium. Nat Rev Microbiol 2019; 17:156–166 [View Article] [PubMed]
    [Google Scholar]
  21. DeStefano Shields CE, Van Meerbeke SW, Housseau F, Wang H, Huso DL et al. Reduction of murine colon tumorigenesis driven by enterotoxigenic Bacteroides fragilis using cefoxitin tMurine Colon Tumorigenesis Driven by Enterotoxigenic Bacteroides fragilis Using Cefoxitin Treatment. J Infect Dis 2016; 214:122–129 [View Article] [PubMed]
    [Google Scholar]
  22. Nakatsu G, Li X, Zhou H, Sheng J, Wong SH et al. Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat Commun 2015; 6:8727 [View Article] [PubMed]
    [Google Scholar]
  23. Loke MF, Chua EG, Gan HM, Thulasi K, Wanyiri JW et al. Metabolomics and 16S rRNA sequencing of human colorectal cancers and adjacent mucosa. PLoS One 2018; 13:e0208584 [View Article] [PubMed]
    [Google Scholar]
  24. Hale VL, Jeraldo P, Chen J, Mundy M, Yao J et al. Distinct microbes, metabolites, and ecologies define the microbiome in deficient and proficient mismatch repair colorectal cancers. Genome Med 2018; 10:78 [View Article] [PubMed]
    [Google Scholar]
  25. Lagier J-C, Khelaifia S, Alou MT, Ndongo S, Dione N et al. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 2016; 1:16203 [View Article] [PubMed]
    [Google Scholar]
  26. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA et al. Culturing of “unculturable” human microbiota reveals novel taxa and extensive sporulation. Nature 2016; 533:543–546 [View Article] [PubMed]
    [Google Scholar]
  27. Dubourg G, Baron S, Cadoret F, Couderc C, Fournier P-E et al. From culturomics to clinical microbiology and forward. Emerg Infect Dis 2018; 24:1683–1690 [View Article] [PubMed]
    [Google Scholar]
  28. Marchesi JR, Dutilh BE, Hall N, Peters WHM, Roelofs R et al. Towards the human colorectal cancer microbiome. PLoS One 2011; 6:e20447 [View Article] [PubMed]
    [Google Scholar]
  29. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE et al. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 2012; 10:575–582 [View Article] [PubMed]
    [Google Scholar]
  30. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012; 22:299–306 [View Article] [PubMed]
    [Google Scholar]
  31. Vancanneyt M, Segers P, Torck U, Hoste B, Bernardet J-F et al. Reclassification of Flavobacterium odoratum (Stutzer 1929) strains to a new genus, Myroides, as Myroides odoratus comb. nov. and Myroides odoratimimus sp. nov. Int J Syst Bacteriol 1996; 46:926–932 [View Article]
    [Google Scholar]
  32. Benedetti P, Rassu M, Pavan G, Sefton A, Pellizzer G et al. Septic shock, pneumonia, and soft tissue infection due to Myroides odoratimimus: report of a case and review of Myroides infections. Infection 2011; 39:161–165 [View Article] [PubMed]
    [Google Scholar]
  33. Maraki S, Sarchianaki E, Barbagadakis S. Myroides odoratimimus soft tissue infection in an immunocompetent child following a pig bite: case report and literature review. Braz J Infect Dis 2012; 16:390–392 [View Article] [PubMed]
    [Google Scholar]
  34. Ktari S, Mnif B, Koubaa M, Mahjoubi F, Ben Jemaa M et al. Nosocomial outbreak of Myroides odoratimimus urinary tract infection in a Tunisian hospital. J Hosp Infect 2012; 80:77–81 [View Article] [PubMed]
    [Google Scholar]
  35. Johansen JE, Nielsen P, Sjøholm C. Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola gen. nov., sp. nov. and reclassification of [Cytophaga] lytica to Cellulophaga lytica gen. nov., comb. nov. Int J Syst Bacteriol 1999; 49 Pt 3:1231–1240 [View Article]
    [Google Scholar]
  36. Holmfeldt K, Middelboe M, Nybroe O, Riemann L et al. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl Environ Microbiol 2007; 73:6730–6739 [View Article] [PubMed]
    [Google Scholar]
  37. Dang VT, Howard-Varona C, Schwenck S, Sullivan MB et al. Variably lytic infection dynamics of large Bacteroidetes podovirus phi38:1 against two Cellulophaga baltica host strains. Environ Microbiol 2015; 17:4659–4671 [View Article] [PubMed]
    [Google Scholar]
  38. Han Z, Zhang Y, Yang J. Biochemical Characterization of a New β-Agarase from Cellulophaga algicola. Int J Mol Sci 2019; 20:E2143 [View Article] [PubMed]
    [Google Scholar]
  39. Valdehuesa KNG, Ramos KRM, Moron LS, Lee I, Nisola GM et al. Draft genome sequence of newly isolated agarolytic bacteria Cellulophaga omnivescoria sp. nov. W5C carrying several gene loci for marine polysaccharide degradation. Curr Microbiol 2018; 75:925–933 [View Article] [PubMed]
    [Google Scholar]
  40. Ramos KRM, Valdehuesa KNG, Nisola GM, Lee W-K, Chung W-J et al. Identification and characterization of a thermostable endolytic β-agarase Aga2 from a newly isolated marine agarolytic bacteria Cellulophaga omnivescoria W5C. N Biotechnol 2018; 40:261–267 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001523
Loading
/content/journal/jmm/10.1099/jmm.0.001523
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error